Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae)

SUMMARYClimate change is causing winters to become milder (less cold and shorter). Recent studies of overwintering ectotherms have suggested that warmer winters increase metabolism and decrease winter survival and subsequent fecundity. Energetic constraints (insufficient energy stores) have been hypothesized as the cause of winter mortality but have not been tested explicitly. Thus, alternative sources of mortality, such as winter dehydration, cannot be ruled out. By employing an experimental design that compared the energetics and water content of lizards that died naturally during laboratory winter with those that survived up to the same point but were then sacrificed, we attempt to distinguish among multiple possible causes of mortality. We test the hypothesis that mortality is caused by insufficient energy stores in the liver, abdominal fat bodies, tail or carcass or through excessive water loss. We found that lizards that died naturally had marginally greater mass loss, lower water content, and less liver glycogen remaining than living animals sampled at the same time. Periodically moistening air during winter reduced water loss, but this did not affect survival, calling into question dehydration as a cause of death. Rather, our results implicate energy limitations in the form of liver glycogen, but not lipids, as the primary cause of mortality in overwintering lizards. When viewed through a lens of changing climates, our results suggest that if milder winters increase the metabolic rate of overwintering ectotherms, individuals may experience greater energetic demands. Increased energy use during winter may subsequently limit individual survival and possibly even impact population persistence.

Section: Climate Change Winter Temperatures and Population Persistencementioning

confidence: 68%

Section: Climate Change Winter Temperatures and Population Persistencementioning

confidence: 99%

Section: Introductionmentioning

confidence: 96%

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Glycogen, not dehydration or lipids, limits winter survival of side-blotched lizards (Uta stansburiana)

Zani

Irwin

Rollyson

et al. 2012

“…Even during metabolic depression, diapausing insects may exhaust fuel stores vital for successful completion of development following winter (Hahn and Denlinger, 2011). Events that increase winter temperatures, such as transient warm fronts that melt insulating snow layers, may be particularly important, causing short periods of intense metabolic demand (Irwin and Lee, 2000;Williams et al, 2012a,b). However, there is evidence for active suppression of temperature-elevated metabolism during winter in insects (Williams et al, 2015).…”

Section: Post-winter Transcriptional Repressionmentioning

confidence: 99%

Divergence of the diapause transcriptome in apple maggot flies: winter regulation and post-winter transcriptional repression

Meyers

Powell

Walden

et al. 2016

The duration of dormancy regulates seasonal timing in many organisms and may be modulated by day length and temperature. Though photoperiodic modulation has been well studied, temperature modulation of dormancy has received less attention. Here, we leverage genetic variation in diapause in the apple maggot fly, Rhagoletis pomonella, to test whether gene expression during winter or following spring warming regulates diapause duration. We used RNAseq to compare transcript abundance during and after simulated winter between an apple-infesting population and a hawthorn-infesting population where the apple population ends pupal diapause earlier than the hawthorn-infesting population. Marked differences in transcription between the two populations during winter suggests that the 'early' apple population is developmentally advanced compared with the 'late' hawthorn population prior to spring warming, with transcripts participating in growth and developmental processes relatively up-regulated in apple pupae during the winter cold period. Thus, regulatory differences during winter ultimately drive phenological differences that manifest themselves in the following summer. Expression and polymorphism analysis identify candidate genes in the Wnt and insulin signaling pathways that contribute to population differences in seasonality. Both populations remained in diapause and displayed a pattern of up-and then down-regulation (or vice versa) of growth-related transcripts following warming, consistent with transcriptional repression. The ability to repress growth stimulated by permissive temperatures is likely critical to avoid mismatched phenology and excessive metabolic demand. Compared with diapause studies in other insects, our results suggest some overlap in candidate genes/pathways, though the timing and direction of changes in transcription are likely species specific.

“…For example, reproductive output of female goldenrod gall flies is determined by lipid reserves remaining in the spring (Irwin and Lee, 2000). Because metabolism of ectotherms (and many hibernating mammals) is determined by the ambient temperature, overwinter energetics can mediate the relationship between environmental conditions and the persistence and performance of populations, and therefore the geographic distribution of animals (Humphries et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Real-time measurement of metabolic rate during freezing and thawing of the wood frog,Rana sylvatica: implications for overwinter energy use

Sinclair

Stinziano

Williams

et al. 2013

109

SUMMARYEctotherms overwintering in temperate ecosystems must survive low temperatures while conserving energy to fuel post-winter reproduction. Freeze-tolerant wood frogs, Rana sylvatica, have an active response to the initiation of ice formation that includes mobilising glucose from glycogen and circulating it around the body to act as a cryoprotectant. We used flow-through respirometry to measure CO 2 production (V CO2 ) in real time during cooling, freezing and thawing. CO 2 production increases sharply at three points during freeze-thaw: at +1°C during cooling prior to ice formation (total of ). We interpret these increases in metabolic rate to represent the energetic costs of preparation for freezing, the response to freezing and the re-establishment of homeostasis and repair of damage after thawing, respectively. We assumed that frogs metabolise lipid when unfrozen and that carbohydrate fuels metabolism during cooling, freezing and thawing, and when frozen. We then used microclimate temperature data to predict overwinter energetics of wood frogs. Based on the freezing and melting points we measured, frogs in the field were predicted to experience as many as 23 freeze-thaw cycles in the winter of our microclimate recordings. Overwinter carbohydrate consumption appears to be driven by the frequency of freeze-thaw events, and changes in overwinter climate that affect the frequency of freeze-thaw will influence carbohydrate consumption, but changes that affect mean temperatures and the frequency of winter warm spells will modify lipid consumption. Supplementary material available online at